Dehaene 2006 Conscious, Preconscious Trends in Cognitive Neuroscience

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Conscious, preconscious, and subliminal processing: a testable taxonomy Stanislas Dehaene 1,2 , Jean-Pierre Changeux 2,3 , Lionel Naccache 1 , Je ´ro ˆ me Sackur 1 and Claire Sergent 1 1 INSERM-CEA Cognitive Neuroimaging Unit, Service Hospitalier Fre ´de ´ ric Joliot, Orsay, France 2 Colle ` ge de France, Paris, France 3 CNRS Unit, Receptors and Cognition, Institut Pasteur, Paris, France Of the many brain events evoked by a visual stimulus, which are specifically associated with conscious percep- tion, and which merely reflect non-conscious processing? Several recent neuroimaging studies have contrasted conscious and non-conscious visual processing, but their results appear inconsistent. Some support a correlation of conscious perception with early occipital events, others with late parieto-frontal activity. Here we attempt to make sense of these dissenting results. On the basis of the global neuronal workspace hypothesis, we propose a taxonomy that distinguishes between vigilance and access to conscious report, as well as between sub- liminal, preconscious and conscious processing. We suggest that these distinctions map onto different neural mechanisms, and that conscious perception is system- atically associated with surges of parieto-frontal activity causing top-down amplification. Introduction Understanding the neuronal mechanisms of conscious- ness is a major challenge for cognitive neuroscience. Recently, great progress has been achieved by contrasting brain activation images obtained during minimally different experimental conditions, one of which leads to conscious perception while the other does not. Surpris- ingly, however no coherent picture has emerged from those experiments. On the contrary, a controversy has arisen, as some studies suggest that consciousness depends mostly on the thalamus and brain stem [1], others on early visual areas [2,3], and yet others on higher prefrontal and parietal association areas [4–9]. Here, we propose that those apparent contradictions can be resolved by a relevant theorizing of the physiologi- cal conditions for conscious processing of sensory stimuli. Based on the recent proposal of a large-scale thalamo- cortical formal network and its simulations [4,5], we tentatively propose a plausible and testable taxonomy of brain activity states associated with conscious and non- conscious processing. In particular, within non-conscious processing, we distinguish a transient ‘preconscious’ state of activity in which information is potentially accessible, yet not accessed. An enabling condition: vigilance The term ‘consciousness’ has multiple meanings, one of them intransitive (e.g. ‘the patient regained conscious- ness’), and the other transitive (e.g. ‘consciousness of color’). To avoid further confusion, we abandon the term and use ‘states of vigilance’ to refer to the non-transitive meaning, i.e. a continuum of states which encompasses wakefulness, sleep, coma, anesthesia, etc. Being in an appropriate state of vigilance (e.g. awake rather than asleep) is an obvious enabling condition for conscious processing of sensory stimuli. Empirically, awakening into the vigilant state correlates with a progressive increase in regional cerebral blood flow, first in the brainstem and thalamus, then in the cortex with a particularly important increase in prefrontal-cingulate activation and functional connectivity [10]. Anesthesia, sleep, vegetative state and coma [1,11] are all associated with modulations of the activity of this large-scale thalamocortical network which also shows high baseline activity during vigilant rest [12] and encompasses prefrontal, cingulate and inferior parietal nodes. These observations may be captured by a recent implementation of the neural workspace model [4] in which ascending brain stem nuclei (e.g. cholinergic among others) send globally depolarizing neuromodulatory sig- nals to a thalamic and cortical hierarchy. Simulations show a progressive increase in spontaneous firing as a function of neuromodulator release, which evolves into what is known in dynamical systems theory as a Hopf bifurcation: spontaneous firing increases continuously in intensity, but high-frequency oscillations appear suddenly in the gamma band (20–80 Hz). By increasing spon- taneous activity, and thus bringing a broad thalamo- cortical network closer to firing threshold, vigilance lowers the threshold for external sensory inputs. In summary, vigilance is a graded variable, and a minimum level is essential for placing thalamo-cortical systems into a receptive state. Corresponding author: Dehaene, S. ([email protected]). Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 www.sciencedirect.com 1364-6613/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2006.03.007

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Transcript of Dehaene 2006 Conscious, Preconscious Trends in Cognitive Neuroscience

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    Several recent neuroimaging studies have contrastedconscious and non-conscious visual processing, but theirresults appear inconsistent. Some support a correlation

    in the brainstem and thalamus, then in the cortex with aparticularly important increase in prefrontal-cingulate

    activity during vigilant rest [12] and encompasses

    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006conscious processing. In particular, within non-consciousdifferent experimental conditions, one of which leads toconscious perception while the other does not. Surpris-ingly, however no coherent picture has emerged fromthose experiments. On the contrary, a controversy hasarisen, as some studies suggest that consciousnessdepends mostly on the thalamus and brain stem [1],others on early visual areas [2,3], and yet others on higherprefrontal and parietal association areas [49].

    Here, we propose that those apparent contradictionscan be resolved by a relevant theorizing of the physiologi-cal conditions for conscious processing of sensory stimuli.Based on the recent proposal of a large-scale thalamo-cortical formal network and its simulations [4,5], wetentatively propose a plausible and testable taxonomy ofbrain activity states associated with conscious and non-

    prefrontal, cingulate and inferior parietal nodes.These observations may be captured by a recent

    implementation of the neural workspace model [4] inwhich ascending brain stem nuclei (e.g. cholinergic amongothers) send globally depolarizing neuromodulatory sig-nals to a thalamic and cortical hierarchy. Simulationsshow a progressive increase in spontaneous firing as afunction of neuromodulator release, which evolves intowhat is known in dynamical systems theory as a Hopfbifurcation: spontaneous firing increases continuously inintensity, but high-frequency oscillations appear suddenlyin the gamma band (2080 Hz). By increasing spon-taneous activity, and thus bringing a broad thalamo-cortical network closer to firing threshold, vigilance lowersthe threshold for external sensory inputs.brain activation images obtained during minimally

    Recently, great progress has been achieved by contrasting thalamocortical network which also shows high baselineof conscious perception with early occipital events,others with late parieto-frontal activity. Here we attemptto make sense of these dissenting results. On the basis ofthe global neuronal workspace hypothesis, we propose ataxonomy that distinguishes between vigilance andaccess to conscious report, as well as between sub-liminal, preconscious and conscious processing. Wesuggest that these distinctions map onto different neuralmechanisms, and that conscious perception is system-atically associated with surges of parieto-frontal activitycausing top-down amplification.

    IntroductionUnderstanding the neuronal mechanisms of conscious-ness is a major challenge for cognitive neuroscience.Conscious, preconssubliminal processitaxonomyStanislas Dehaene1,2, Jean-Pierre Changeand Claire Sergent1

    1INSERM-CEA Cognitive Neuroimaging Unit, Service Hospitalie2Colle`ge de France, Paris, France3CNRS Unit, Receptors and Cognition, Institut Pasteur, Paris, Fra

    Of the many brain events evoked by a visual stimulus,which are specifically associated with conscious percep-tion, andwhichmerely reflectnon-conscious processing?activation and functional connectivity [10]. Anesthesia,sleep, vegetative state and coma [1,11] are all associatedwith modulations of the activity of this large-scaleious, andg: a testable

    2,3, Lionel Naccache1, Jerome Sackur1

    ederic Joliot, Orsay, France

    e

    processing, we distinguish a transient preconscious stateof activity in which information is potentially accessible,yet not accessed.

    An enabling condition: vigilanceThe term consciousness has multiple meanings, one ofthem intransitive (e.g. the patient regained conscious-ness), and the other transitive (e.g. consciousness ofcolor). To avoid further confusion, we abandon the termand use states of vigilance to refer to the non-transitivemeaning, i.e. a continuum of states which encompasseswakefulness, sleep, coma, anesthesia, etc.

    Being in an appropriate state of vigilance (e.g. awakerather than asleep) is an obvious enabling condition forconscious processing of sensory stimuli. Empirically,awakening into the vigilant state correlates with aprogressive increase in regional cerebral blood flow, firstminimum level is essential for placing thalamo-corticalsystems into a receptive state.

    Corresponding author: Dehaene, S. ([email protected]).

    www.sciencedirect.com 1364-6613/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2006.03.007In summary, vigilance is a graded variable, and a

  • visibility are found solely in occipital areas, not in higherassociative regions, and therefore argue that the mech-

    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 205Early visual activation is not sufficientfor conscious reportWe now consider the neural bases of the second, transitivemeaning of consciousness, which we term access toconscious report. How do we consciously perceive a visualstimulus? Many neuroimaging experiments have demon-strated a tight correlation between the conscious visualperception and the activation of striate and extrastriatevisual areas [1318]. For instance, unmasking of a visualstimulus increases activity in extrastriate areas in tightcorrelation with subjective reports of stimulus visibility[18]. Furthermore, extrastriate regions clearly play acausal role in conscious visual perception, because theirselective lesioning eliminates the corresponding contentsfrom experience for instance a lesion of area V4 candestroy color perception in the contralateralhemifield [19].

    On the basis of such data, Zeki [2] has proposed that theconscious perception of a given visual attribute resides inthe extrastriate area specialized for that attribute (e.g.area MT/V5 for motion, or area V4 for color). A micro-consciousness would be involved whenever that areareceives a sufficient amount of activation.

    We argue, however, that early sensory activation isnecessary but not sufficient for conscious access, becauseactivity in extrastriate visual areas is frequently observedwhile participants deny having seen any stimulus [14,2023]. When invisibility is caused by masking [20] or bydichoptic stimulation [14] this stimulus-evoked activityremains weak, and one might argue that its smallamplitude alone could explain the absence of consciousperception [2,14]. However, the visual activation evokedby invisible stimuli can also be very strong, for instancewhen invisibility is caused by neglect [21] or inattention[22,23]. In a recent study of the attentional blink, weobserved that up to about 180 ms after stimulus presen-tation, the occipito-temporal event-related potentialsevoked by a invisible word were large and essentiallyindistinguishable from those evoked by a visible word [23].Yet on invisible trials, the participants visibility ratingsdid not deviate from the lowest value, used when no wordwas physically present. Thus, intense occipito-temporalactivation can be accompanied by a complete lack ofconscious report.

    Top-down amplification, long-distance reverberation,and reportabilityWe [46] and others [7,8,24] have suggested that, inaddition to vigilance and bottom-up activation, a thirdfactor underlying conscious access is the extension ofbrain activation to higher association cortices intercon-nected by long-distance connections and forming areverberating neuronal assembly with distant perceptualareas. Why would this brain state correspond to consciousaccess? Neurocomputational simulations show that oncestimulus-evoked activation has reached highly intercon-nected associative areas, two important changes occur: (1)The activation can reverberate, thus holding informationon-line for a long duration essentially unrelated to the

    initial stimulus duration; (2) Stimulus information can berapidly propagated to many brain systems. We argue that

    www.sciencedirect.comanisms of conscious visual perception lie inextrastriate cortex.

    We obviously agree on one point: it is important todesign paradigms in which conscious perception is notconfounded with massive changes in overt or covertbehaviour. However, this goal has been achieved in severalstudies. In our recent study of the attentional blink [23],for instance, subjects viewed a fixed stimulus and madesimilar motor gestures on seen and not-seen trials, yetthose were still distinguished by strong parieto-frontal activation.

    We question, however, the proposal that inattention isan appropriate control. Under conditions of divertedattention, such as those studied by Tse et al. [18], evenan unmasked stimulus is not guaranteed to be consciouslyperceived. On the contrary, considerable evidence indi-cates that without attention, conscious perception cannotoccur. In the inattentional blindness paradigm, even a700-ms stimulus presented in the fovea, when unat-tended, might fail to be seen [33]. During the attentionalblink, a mildly masked stimulus, normally quite visible,both properties are characteristic of conscious informationprocessing which in our view is associated with a distinctinternal space, buffered from fast fluctuations in sensoryinputs, where information can be shared across a broadvariety of processes including evaluation, verbal report,planning and long-term memory [25].

    Empirically, access of sensory stimuli to consciousreport correlates with the activation of higher associativecortices, particularly parietal, prefrontal and anteriorcingulate areas. In fMRI, the activation of those regionssystematically separates masked versus unmasked pre-sentations of words [20] or images [26]; undetected versusdetected changes during change blindness [27,28]; extin-guished versus seen visual stimuli in neglect patients [29];or missed versus reported stimuli during the attentionalblink [9,22,23,3032]. In many of these paradigms,anterior activation is accompanied by an amplificationand an increase in functional correlation with posteriorstimulus-specific areas [20,26,30]. Sudden parieto-frontalactivation and top-down amplification are two frequentsignatures of conscious perception.

    Is attention a confound or a necessity for consciousaccess?Some have argued that many of the above neuroimagingparadigms are inappropriately controlled because con-scious perception is confounded with increased attentionand more extended stimulus processing. For instance, aconscious word can be attended, repeated or memorizedwhile a non-conscious word cannot. Such confounds wouldsuffice to explain the greater parieto-prefrontal activity tounmasked words [20]. For this reason, Tse et al. [18] haveargued that one should prefer experimental designs inwhich attention is drawn away from the stimulus. Theyshow that, in such a situation, correlates of stimulusbecomes invisible when attention is diverted to anothertask [23,34].

  • The relations between stimulus strength, attention,and conscious perception are complex because attentionmechanisms can also be activated automatically in abottom-up manner. When the stimuli have strong energy,sharp onsets or strong emotional content, they mighttrigger an activation of frontal eye fields or amygdalapathways, thus causing an amplification that can lowertheir threshold for conscious perception [35]. Thus, bothbottom-up stimulus strength and top-down attentionalamplification (whether triggered voluntarily or by auto-matic attraction) are jointly needed for conscious percep-tion, but they might not always be sufficient for astimulus to cross the threshold for conscious perception.Conscious perception must therefore be evaluated bysubjective report, preferably on a trial-by-trial basis.Verifying that the stimuli can be consciously perceived ina separate experimental block where they are attended,as done by Tse et al. [18], does not suffice to guaranteeconscious perception in a different block where attentionis diverted. One cannot simply assume that, by

    unmasking stimuli, one is studying the neural correlatesof conscious processing.

    Distinguishing accessibility from accessThe above distinctions lead us to proposal a formaldefinition of two types of non-conscious processes(Figure 1):

    (1) Subliminal processing. We define subliminal proces-sing (etymologically below the threshold) as acondition of information inaccessibility where bot-tom-up activation is insufficient to trigger a large-scalereverberating state in a global network of neuronswith long range axons. Simulations of a minimalthalamo-cortical network [4] indicates that such a non-linear self-amplifying system possesses a well-defineddynamical threshold. A processing stream thatexceeds a minimal activation level quickly growsuntil a full-scale ignition is seen, while a slightly

    Top-down attention

    Absent PresentBottom-upstimulusstrength

    Weakor

    interrupted

    Subliminal (unattended) Subliminal (attended) Very little activation Activation is already weak in early extrastriate areas Little or no priming No reportability

    Strong feedforward activation Activation decreases with depth Depth of processing depends on attention and task set Activation can reach semantic level Short-lived priming No durable fronto- parietal activity No reportability

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    tation of top-down attention to the stimulus, or away from it (task-unrelated attention).

    a sharp transition between states. During subliminal processing, activation propagates

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    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006206Sufficientlystrong

    Preconscious Intense activation, yet confined to sensori-motor processors Occipito-temporal loops and local synchrony Priming at multiple levels No reportability while attention is occupied elsewhere

    Figure 1. Proposed distinction between subliminal, preconscious, and conscious pro

    up stimulus strength (on the vertical axis at left) and top-down attention (on the hori

    arrows the interactions among them. Large arrows schematically illustrate the orien

    Dashed curves indicate a continuum of states, and thick lines with separators indicate

    but remains weak and quickly dissipating (decaying to zero after 12 seconds). A

    attention, and instructions (see Box 1). During preconscious processing, activation c

    frontal eye fields). However, when attention is oriented away from the stimulus (lar

    establishing long-distance synchrony. During conscious processing, activation invabecomes capable of guiding intentional actions including verbal reports. The transition

    self-amplified non-linear system [4].

    www.sciencedirect.comtinuum of subliminal states can exist, depending on masking strength, top-down

    e strong, durable, and can spread to multiple specialized sensori-motor areas (e.g.

    lack arrows), activation is blocked from accessing higher parieto-frontal areas and

    a parieto-frontal system, can be maintained ad libidum in working memory, andTRENDS in Cognitive Sciences

    Conscious Orientation of top-down attention Amplification of sensori-motor activity Intense activation spreading to parieto- frontal network Long-distance loops and global synchrony Durable activation, maintained at will Conscious reportability

    ing. Three types of brain states are schematically shown, jointly defined by bottom-

    tal axis). Shades of color illustrate the amount of activation in local areas, and smallbetween preconscious and conscious is sharp, as expected from the dynamics of a

  • weaker activation quickly dies out. Subliminal proces-sing corresponds to the latter type.

    Note that, under our hypothesis, subliminal processingis not confined to a passive spreading of activation,independent of the subjects attention and strategies, aspreviously envisaged. On the contrary, whichever taskand attentional set are prepared consciously can orientand amplify the processing of a subliminal stimulus, evenif its bottom-up strength remains insufficient for globalignition. In agreement with this analysis, many top-downinfluences on subliminal processing have now beenexperimentally observed (Box 1).

    (2) Preconscious processing. Freud [36] noted that someprocesses [.] may cease to be conscious, but canbecome conscious once more without any trouble, andhe proposed that everything unconscious that behavesin this way, that can easily exchange the unconsciouscondition for the conscious one, is therefore betterdescribed as capable of entering consciousness or aspreconscious.

    Here we further specify the latter term. We propose tocall preconscious (or potentially conscious, or P-conscious)

    Box 1. Why attention and consciousness are different: top-

    down influences on subliminal processing

    Subliminal processing is frequently thought to be automatic andindependent of attention. However, the present framework impliesthat top-down attention and task set can have an effect on subliminalprocessing (see Figure 1 in main text, top row). This prediction hasbeen verified in several recent reports.

    Modulation of subliminal priming by temporal attentionIn a numerical masked priming paradigm, Naccache et al. [43] firstshowed that subliminal priming was present when subjects couldallocate attention to the prime-target pair, but vanished when

    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 207stimuli could not be temporally attended. Kiefer and Brendel [44]observed a similar effect in an experiment investigating the N400potential elicited by masked words. Unseen masked words eliciteda much larger N400 when they were temporally attended than whenthey were not.

    Modulation by spatial attentionKentridge et al. [45,46] first reported that blindsight patient GY coulduse consciously perceived cues to enhance unconscious processingof visual targets. When a target was presented in his blind visualfield, GY responded faster and more accurately when it was validlycued by a consciously perceptible arrow pointing to it, than when itwas invalidly cued. In both cases, he still claimed that he could notsee the target. Modulation of subliminal priming by spatial attentionwas also observed in normal subjects [47].

    Modulation by strategiesTask instructions also alter the fate of subliminal stimuli. Forinstance, masked primes can elicit instruction-dependent activationin motor cortex [48,49], suggesting that arbitrary stimulusresponsemappings conveyed by conscious instructions can also apply to non-conscious stimuli. The influence is always unidirectional: once astrategy or response mapping is consciously adopted, it extends tonon-conscious primes [50,51]. Kunde et al. [51] studied the Grattoneffect, a strategic increase in executive control that follows Stroopinterference trials. They observed this effect following consciousconflict trials, but not following subliminal conflict trials. Onceestablished, however, the increase in control applied to both

    subliminal and supraliminal trials another instance of a top-downeffect on subliminal processing.

    www.sciencedirect.coma neural process that potentially carries enough activationfor conscious access, but is temporarily buffered in a non-conscious store because of a lack of top-down attentionalamplification (for example, owing to transient occupancyof the central workspace system). As shown by theattentional blink and inattentional blindness paradigms,even strong visual stimuli can remain temporarilypreconscious. They are potentially accessible (they couldquickly gain access to conscious report if they wereattended), but they are not consciously accessed atthe moment.

    At the neurocomputational level, preconscious proces-sing is proposed to involve resonant loops within mediumrange connections which maintain the representation ofthe stimulus temporarily active in a sensory buffer for afew hundred milliseconds. A preconscious stimulus mightultimately achieve conscious access once the centralworkspace is freed (as exemplified by the psychologicalrefractory period paradigm [37,38], in which one task isput on hold while another task is being processed). Itmight never gain access to conscious processing if thepreconscious buffer is erased before the orienting of top-down attention (as achieved by masking in the attentionalblink paradigm).

    Accounting for conflicting neuroimaging dataIn experimental studies of conscious perception, precon-scious processing, as an intermediate category, has some-times been confounded with subliminal processing, andsometimes with conscious processing. We now show howthis distinction can provide a simple account of conflictingneuroimaging results (Figure 2).

    (1) Masking when stimuli are attended. Some exper-iments require participants to attend to maskedstimuli which are made visible or invisible bychanging the masking strength. In our taxonomy,those experiments contrast subliminal versus con-scious stimuli a major contrast which should revealboth early stimulus processing regions and a dis-tributed parieto-frontal workspace system. Indeed,empirically, both early extrastriate and late parietaland prefrontal differences have been observed [20,26].

    (2) Stimuli presented at threshold. Even when attended,stimuli presented at sensory threshold may or may notbe perceived. In our theory this is again a contrastbetween subliminal and conscious stimuli. As pre-dicted, neuroimaging experiments relying on thiscontrast have yielded both early (e.g. P100) and late(e.g. P300) correlates of conscious perception[15,16,39]. The theory can also explain why consciousaccess fluctuates even though the stimulus remainsconstant. Simulations show that the threshold forglobal ignition can vary both with vigilance and withthe amount of spontaneous activity before stimuluspresentation [4]. Several experiments confirm that theperception of near-threshold stimuli can be predictedby the prestimulus state, in both humans andmonkeys [40,41].(3) Masking when stimuli are not attended. If stimuli arenot attended, then the comparison of masked and

  • 1 ve

    T2

    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006208Globalworkspace

    T1Conscious

    high strengthand attention

    TT2Preconscioushigh strength,no attention

    T3Subliminal

    weak strength(a) (b)unmasked stimuli becomes a contrast between sub-liminal and preconscious processing. As predicted,only the early components of occipito-temporal acti-vation are seen [18]. According to our terminology,these are the correlates of preconscious visual proces-sing (potential visibility, yet no conscious access).

    (4) Stimuli made invisible by inattention. Some exper-iments have contrasted consciously perceived stimuliwith stimuli made invisible by diverting top-downattention (attentional blink, change blindness, inat-tentional blindness). This is a contrast betweenpreconscious and conscious processing. As expected,the difference appears late (200300 ms after thestimulus) and involves parieto-prefrontal activationas well as late amplification of posterior activity[22,23,2630,32].

    ConclusionInstead of the classical binary separation between non-conscious and conscious processing, we introduce here atripartite distinction between subliminal, preconscious,and conscious processing. The key idea is that, within non-conscious states, it makes a major difference whetherstimuli invisibility is achieved by a limitation in bottom-upstimulus strength, or by the temporary withdrawal of

    Seen stim

    Figure 2. Resolving contradictions in neuroimaging studies. (a) Schematic representation

    accessed when it activates, in a synchronized, reciprocal and long-lasting manner, a set o

    cortices, and whose long-distance connections enable broadcasting to many distant are

    enough bottom-up strength, for example, owing to low-level masking or presentation clo

    to be visible, but still fail to be seen by losing the competition for central access relat

    (b) Reinterpretation of neuroimaging experiments in this framework. When masked and

    difference in brain activation is seen, with both early sensory and late parieto-frontal enh

    also [16,26,39]). When masked and unmasked stimuli are contrasted while attention is

    temporal cortices (fMRI data by Kouider and Dehaene; see also [18]). When stimuli ar

    attention to or away from the stimuli (bottom right), the difference in activation is late an

    (illustrations from the attentional blink paradigm reproduced with permission from [23]

    www.sciencedirect.comT1 versus T3: unmasked or masked stimuli(both attended)

    rsus T2: accessed versus non-accessed stimuli

    Unmasked words (T1) Masked words (T3)

    Unmasked words (T2)>

    masked words (T3)(both used as unattended primes)

    versus T3: unmasked versus masked stimuli(both unattended)top-down attention. The first case corresponds to sub-liminal processing, the second to preconscious processing.We have shown how this distinction is theoreticallymotivated and helps make sense of neuroimaging data.

    Is our taxonomy complete? Box 2 briefly discusses threeother types of non-conscious knowledge in the nervoussystem: latent connectivity patterns, distributed firingpatterns, and functionally disconnected brain systems.Altogether, these distinctions might suffice to capture theknown experimental conditions in which informationescapes conscious reportability. The proposed taxonomyis testable, not only with neuroimaging tools, but alsousing electrophysiological techniques in the awakemonkey, provided that tasks similar to the attentionalblink and psychological refractory period can be developedin these species (see Box 3).

    Our proposal could also lead to a reconciliation of severalmajor theories of conscious perception. The distinctionbetween preconscious and conscious processing is consist-ent with Lammes proposal of a progressive build-up ofrecurrent interactions, first locally within the visualsystem, and second more globally into parieto-frontalregions [3]. It is also consistent with Zekis hypothesis ofan asynchronous construction of visual perceptionin multiple distributed sites before binding into a

    uli (T1) > missed stimuli (T2) during the attentional blinkof the global neuronal workspace model. A visual target T1 (in green) is consciously

    f central workspace neurons particularly dense in parietal, prefrontal and cingulate

    as. A stimulus can fail to become conscious for two reasons: (1) it might not have

    se to threshold (subliminal stimulus T3, in red); or (2) it might have enough strength

    ive to other concurrent stimuli or task sets (preconscious stimulus T2, in orange).

    unmasked stimuli are contrasted while subjects are attending (top right), a major

    ancements for seen stimuli (illustration reproduced with permission from [20]; see

    drawn elsewhere (middle right), the effect of masking is confined to early occipito-

    e above the masking threshold, and conscious access is manipulated by drawing

    d confined to higher association cortices, particular parietal and prefrontal regions

    left image, and [30] right image); see also [21,22,31].

  • ssible? A hypothetical taxonomy

    workspace hypothesis states that it must be represented by smallgroups of neurons whose firing provides an unambiguous index of therelevant attribute, and which would be amplified by top-downattention. For instance, although the collective firing of V1 neuronsencodes all aspects of the visual scene, including the presence of facesor color, those attributes would not be consciously seen unless theextrastriate areas involved in their extraction are intact. At a highercognitive level, when we gain conscious access to a previouslysubliminal distinction (e.g. development of phonemic awareness inchildren), neuronal populations selective for this learned distinctionshould be found.

    (iii) Information is coded by neurons functionally discon-nected from the workspaceEven information in explicit firing form can remain non-conscious ifthe relevant neurons lack the bidirectional projections appropriateto establish a reverberant assembly with parietal and prefrontalcortices. This functional disconnection hypothesis might explainwhy we have no conscious access to the state of activity ofsubcortical systems sustaining basic maintenance processes (res-piration, ingestion, posture, etc). Patients with white matter lesions,including callosal lesions, can also lose conscious access to word,color or object information that is still extracted, yetfunctionally disconnected.

    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 209Box 2. Why does some knowledge remain permanently inacce

    This article discusses a model of how visual processing can remainnon-conscious for dynamical reasons of insufficient strength orconcurrent attentional load. A complete taxonomy such as thatproposed in Table I, however, should also capture the many types ofpermanentlynon-conscious knowledge stored in the nervous system.The global neuronal workspace hypothesis stipulates that infor-mation is consciously accessible if it is explicitly coded in the firing ofgroups of excitatory neurons with bidirectional links to a distributednetwork of workspace neurons. Accordingly, information mightremain permanently non-conscious for at least three reasons [6]:

    (i) Information is not encoded in neuronal firingKnowledge stored in a latent form as synaptic efficacies remainsinaccessible until it is used to recreate evoked patterns of neural firing.This constraint may explain instances of implicit learning, and why wedo not have conscious access to most of our mental algorithms. In thefew cases where we do (e.g. when we describe the steps needed forlong division), the model predicts that each step should be explicitlycoded in the firing of workspace neurons. Indeed, experimentally,prefrontal neurons coding for intentions, plans, ordinal steps,evaluations, intermediate decisions, and errors have been identified.

    (ii) Information is not represented in explicit firing form [52]For an aspect of the visual scene to be consciously accessible, themacro-consciousness [2]. Our only source of disagreement but an important one resides in their attribution ofphenomenal consciousness or micro-consciousness towhat we have termed pre-conscious processing. Rememberthat, in such a state, only a few hundreds of millisecondsafter a stimulus was presented and yielding strong visualactivity, participants deny perceiving anything [34].Whether they actually had a conscious phenomenalexperience but no possibility of reporting it, does not seemto be, at this stage, a scientifically addressable question.The only rationale for attributing phenomenal conscious-ness to preconscious processing seems to be the intuitionthat visual experience involves a richness of content thatgoes beyond what we can report [42]. However, thisintuition itself can be explained as a kind of illusion wethink that we see more than we actually do (Box 4).

    To further explore these difficult issues in the future, itwill be crucial to develop better methods for the formalcollection and quantification of introspective reports[23,34], as well as for the study of the spontaneous flowof conscious processes [4,12]. Meanwhile, the proposeddistinction between subliminal, preconscious and con-scious processing, and the identification of conscious

    Box 3. Questions for further research

    Can one design attentional blink, psychological refractory period,and partial report paradigms for non-human primates? Can they beused to dissect the neural mechanisms of the preconscious buffer?Does this preconscious state engage solely local occipito-temporalloops? Do all demonstrations of non-conscious information processing inhumans fall into one of the categories of the proposed taxonomy? Inparticular, can one identify model cases where the non-consciousinformation is demonstrably encoded in synaptic weights, or inneural systems functionally disconnected from parieto-frontalareas? Can transcranial magnetic stimulation (TMS) be used to disruptparieto-frontal circuits and probe their causal involvement inconscious visual perception? Would occipito-temporal TMS simi-larly disrupt the preconscious buffer during the psychologicalrefractory period? Can one find experimental means of testing whether anysubjective content is associated with preconscious states? Or isthe existence of non-reportable conscious states untestable bydefinition? Can better non-verbal methods be developed for the quantificationof introspective reports, both in humans and in non-humanprimates? What type of neural activity patterns underlies introspectivereports, as opposed to other more direct sensory-motor decisions?

    Table I. A theoretical taxonomy of conscious and non-conscious information encoding in the brain

    Information encoding Main features

    Non-conscious Latent connectivitypatterns

    Information is encoded in latent form as matrices of synaptic weights

    Distributed firing patterns Information is encoded in the distributed firing of many neurons, not condensedin small specialized groups of neurons

    Functionally disconnectedsystems

    Information is encoded in the firing of neurons functionally disconnected fromthe workspace

    Subliminal processing Processing is confined to a brief travelling pulse of firingPreconscious processing Processing involves local resonant firing loops, but top-down attention is

    focussed on another stimulus or task set.

    Conscious processing Processing receives top-down amplification and expands into a global parieto-frontal reverberant state.

    www.sciencedirect.com

  • attention or occur at an attended location are immediately detected.Thus, the illusion of seeing might arise because viewers know that

    Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006210they can, at will, orient attention to any location and obtainconscious information from it.

    In summary, according to the present terminology, the wholeBox 4. Phenomenal consciousness without reportability?

    Following Weiskrantz [53], we consider that subjective reports are theprimary criterion that can establish whether a percept is conscious ornot. Such reports need not be verbal. Many neuroimaging exper-iments rely on manual reports of conscious perception, which can bemade more precise by the use of a continuous visibility measure[23,34].

    The philosopher Ned Block, however, has suggested that thereportability criterion underestimates conscious contents [42]. Whenwe view a complex visual scene, we experience a richness of contentthat seems to go beyond what we can report. This intuition led Blockto propose a distinct state of phenomenal consciousness prior toglobal access. This proposal receives an apparent confirmation inSperlings iconic memory paradigm. When an array of letters isflashed, viewers claim to see the whole array, although they can laterreport only one subsequently cued row or column. One mightconclude that the initial processing of the array, before attentionalselection of a row or column, is already phenomenally conscious[3,42].

    However, these intuitions are questionable, because viewers areknown to be over-confident and to suffer from an illusion of seeing[54]. The change-blindness paradigm demonstrates this discre-pancy between what we see and what we think we see [55]. In thisparadigm, viewers who claim to perceive an entire visual scene failto notice when an important element of the scene changes. Thissuggests that, at any given moment, very little of the scene isactually consciously processed. Interestingly, changes that attractcontents with globally accessible ones, appear to beproductive avenues for scientific research.

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    Conscious, preconscious, and subliminal processing: a testable taxonomyIntroductionAn enabling condition: vigilanceEarly visual activation is not sufficient for conscious reportTop-down amplification, long-distance reverberation, and reportabilityIs attention a confound or a necessity for conscious access?Distinguishing accessibility from accessAccounting for conflicting neuroimaging dataConclusionReferences